Epigenetic reprogramming rewires transcription during the alternation of generations in Arabidopsis
Abstract
Alternation between morphologically distinct haploid and diploid life forms is a defining feature of most plant and algal life cycles, yet the underlying molecular mechanisms that govern these transitions remain unclear. Here, we explore the dynamic relationship between chromatin accessibility and epigenetic modifications during life form transitions in Arabidopsis. The diploid-to-haploid life form transition is governed by the loss of H3K9me2 and DNA demethylation of transposon-associated cis-regulatory elements. This event is associated with dramatic changes in chromatin accessibility and transcriptional reprogramming. In contrast, the global loss of H3K27me3 in the haploid form shapes a chromatin accessibility landscape that is poised to re-initiate the transition back to diploid life after fertilization. Hence, distinct epigenetic reprogramming events rewire transcription through major reorganization of the regulatory epigenome to guide the alternation of generations in flowering plants.
Data availability
Deep-sequencing data that support the findings of this study have been deposited in the Gene Expression Omnibus (GEO) under accession code GSE155369. Re-analysis of previously published DNA methylomes from dme-2/+ pollen (Ibarra et al., 2012), and siRNAs from leaves (Papareddy et al., 2020) and pollen (Borges et al., 2018; Slotkin et al., 2009) were deposited in the GEO under accession code GSE155369.
-
Epigenetic reprogramming rewires transcription during the alternation of generations in ArabidopsisNCBI Gene Expression Omnibus, GSE155369.
-
Active DNA demethylation in plant companion cells reinforces transposon methylation in gametesNCBI Gene Expression Omnibus, GSE38935.
-
Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatinNCBI Gene Expression Omnibus, GSE120669.
-
Transposon-derived small RNAs triggered by miR845 mediate genome dosage response in ArabidopsisNCBI Gene Expression Omnibus, GSE106117.
-
Epigenetic reprogramming and small RNA silencing of transposable elements in pollenNCBI Gene Expression Omnibus, GSE61028.
Article and author information
Author details
Funding
Austrian Science Fund (P26887)
- Frédéric Berger
Austrian Science Fund (I 4258)
- Frédéric Berger
Austrian Science Fund (I2163-B16)
- Frédéric Berger
Austrian Science Fund (M1818)
- Michael Borg
European Commission (ERC 637888)
- Michael D Nodine
Biotechnology and Biological Sciences Research Council (BB/I011269/1)
- David Twell
Biotechnology and Biological Sciences Research Council (BB/N005090)
- David Twell
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Richard Amasino, University of Wisconsin Madison, United States
Publication history
- Received: August 7, 2020
- Accepted: January 25, 2021
- Accepted Manuscript published: January 25, 2021 (version 1)
- Version of Record published: March 1, 2021 (version 2)
Copyright
© 2021, Borg et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 4,956
- Page views
-
- 760
- Downloads
-
- 26
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Developmental Biology
Natriuretic peptide signaling has been implicated in a broad range of physiological processes, regulating blood volume and pressure, ventricular hypertrophy, fat metabolism, and long bone growth. Here, we describe a completely novel role for natriuretic peptide signaling in the control of neural crest (NC) and cranial placode (CP) progenitors formation. Among the components of this signaling pathway, we show that natriuretic peptide receptor 3 (Npr3) plays a pivotal role by differentially regulating two developmental programs through its dual function as clearance and signaling receptor. Using a combination of MO-based knockdowns, pharmacological inhibitors and rescue assays we demonstrate that Npr3 cooperate with guanylate cyclase natriuretic peptide receptor 1 (Npr1) and natriuretic peptides (Nppa/Nppc) to regulate NC and CP formation, pointing at a broad requirement of this signaling pathway in early embryogenesis. We propose that Npr3 acts as a clearance receptor to regulate local concentrations of natriuretic peptides for optimal cGMP production through Npr1 activation, and as a signaling receptor to control cAMP levels through inhibition of adenylyl cyclase. The intracellular modulation of these second messengers therefore participates in the segregation of NC and CP cell populations.
-
- Developmental Biology
- Evolutionary Biology
Genetic studies in human and mice have established a dual role for Vsx genes in retina development: an early function in progenitors’ specification, and a later requirement for bipolar-cells fate determination. Despite their conserved expression patterns, it is currently unclear to which extent Vsx functions are also conserved across vertebrates, as mutant models are available only in mammals. To gain insight into vsx function in teleosts, we have generated vsx1 and vsx2 CRISPR/Cas9 double knockouts (vsxKO) in zebrafish. Our electrophysiological and histological analyses indicate severe visual impairment and bipolar cells depletion in vsxKO larvae, with retinal precursors being rerouted toward photoreceptor or Müller glia fates. Surprisingly, neural retina is properly specified and maintained in mutant embryos, which do not display microphthalmia. We show that although important cis-regulatory remodelling occurs in vsxKO retinas during early specification, this has little impact at a transcriptomic level. Our observations point to genetic redundancy as an important mechanism sustaining the integrity of the retinal specification network, and to Vsx genes regulatory weight varying substantially among vertebrate species.